ERS statement on harmonised standardsfor lung cancer registration and lungcancer services in Europe
Anna L. Rich1, David R. Baldwin1, Paul Beckett2, Thierry Berghmans3,Jeanette Boyd4, Corinne Faivre-Finn5, Françoise Galateau-Salle6,Fernando Gamarra7, Bogdan Grigoriu3, Niels-Christian G. Hansen8,Georgia Hardavella9,10, Erik Jakobsen11, Dragana Jovanovic12,Assia Konsoulova13, Gilbert Massard14, John McPhelim15, Anne-Pascale Meert3,Robert Milroy16, Luciano Mutti17, Marianne Paesmans18, Michael D. Peake19,20,Paul Martin Putora21,22, Dirk K.M. de Ruysscher23,24, Jean-Paul Sculier3,Arnaud Scherpereel25, Dragan R. Subotic26, Paul Van Schil27 andTorsten Gerriet Blum28
@ERSpublicationsWritten by Europeans for Europeans, this minimum dataset and manual for lung cancer services willhelp to improve standards for our patients http://ow.ly/6qa630mm5bz
Cite this article as: Rich AL, Baldwin DR, Beckett P, et al. ERS statement on harmonised standards forlung cancer registration and lung cancer services in Europe. Eur Respir J 2018; 52: 1800610 [https://doi.org/10.1183/13993003.00610-2018].
ABSTRACT The European Respiratory Society (ERS) task force for harmonised standards for lungcancer registration and lung cancer services in Europe recognised the need to create a single dataset foruse in pan-European data collection and a manual of standards for European lung cancer services.
The multidisciplinary task force considered evidence from two different sources, reviewing existingnational and international datasets alongside the results of a survey of clinical data collection on lungcancer in 35 European countries. A similar process was followed for the manual of lung cancer services,with the task force using existing guidelines and national or international recommendations for lungcancer services to develop a manual of standards for services in Europe.
The task force developed essential and minimum datasets for lung cancer registration to enable allcountries to collect the same essential data and some to collect data with greater detail. The task force alsodeveloped a manual specifying standards for lung cancer services in Europe.
Despite the wide variation in the sociopolitical landscape across Europe, the ERS is determined toencourage the delivery of high-quality lung cancer care. Both the manual of lung cancer services and theminimum dataset for lung cancer registration will support this aspiration.
Published online Dec 20, 2018; republished May 15, 2019 with a correction to a typographical error in one of the authornames (A. Scherpereel).
This article has supplementary material available from erj.ersjournals.com
This document was endorsed by the ERS Science Council and Executive Committee on September 19, 2018.
Received: March 29 2018 | Accepted after revision: July 03 2018
Affiliations: 1Dept of Respiratory Medicine, Nottingham University Hospitals NHS Trust, Nottingham, UK.2Dept of Respiratory Medicine, Derby Teaching Hospitals NHS Foundation Trust, Derby, UK. 3Intensive Careand Thoracic Oncology, Institut Jules Bordet, Université Libre de Bruxelles, Brussels, Belgium. 4EuropeanLung Foundation, Sheffield, UK. 5Division of Cancer Sciences, University of Manchester and The Christie NHSFoundation Trust, Manchester, UK. 6Dept of Biopathology, MESOPATH/MESOBANK Cancer Center LeonBerard, Lyon, France. 7Sektion Pneumologie, Klinikum St. Elisabeth, Straubing, Germany. 8Dept ofRespiratory Medicine, Odense University Hospital, Odense, Denmark. 9Dept of Respiratory Medicine, King’sCollege Hospital London, London, UK. 10Dept of Respiratory Medicine and Allergy, King’s College London,London, UK. 11Dept of Thoracic Surgery, Odense University Hospital, Odense, Denmark. 12University Hospitalof Pulmonology, Clinical Center of Serbia, Belgrade, Serbia. 13Medical Oncology Clinic, University Hospital“Sveta Marina”, Varna, Bulgaria. 14Service de Chirurgie Thoracique, Hôpitaux Universitaires de Strasbourg,Strasbourg, France. 15Hairmyres Hospital, NHS Lanarkshire, East Kilbride, UK. 16Scottish Lung CancerForum, Glasgow Royal Infirmary, Glasgow, UK. 17Biomedical Research Centre, University of Salford, Salford,UK. 18Data Centre, Institut Jules Bordet, Université Libre de Bruxelles, Brussels, Belgium. 19University ofLeicester, Leicester, UK. 20University College London Hospitals, London, UK. 21Dept of Radiation Oncology,Kantonsspital St Gallen, St Gallen, Switzerland. 22Dept of Radiation Oncology, University of Bern, Bern,Switzerland. 23Maastricht University Medical Center, Dept of Radiation Oncology (Maastro Clinic), GROWSchool for Oncology and Developmental Biology, Maastricht, The Netherlands. 24Radiation Oncology, KULeuven, Leuven, Belgium. 25Pulmonary and Thoracic Oncology, Université de Lille, Inserm, CHU Lille, Lille,France. 26Dept of Thoracic Surgery, University Hospital, Basel, Switzerland. 27Dept of Thoracic and VascularSurgery, Antwerp University Hospital, Edegem (Antwerp), Belgium. 28Klinik für Pneumologie, LungenklinikHeckeshorn, HELIOS Klinikum Emil von Behring, Berlin, Germany.
Correspondence: Anna L. Rich, Dept of Respiratory Medicine, Nottingham University Hospitals NHS Trust,City Campus, Hucknall Road, Nottingham, NG5 1PB, UK. E-mail: [email protected]
IntroductionLung cancer is the second most common cancer in men and women in Europe and the commonest causeof cancer-related death [1]. Europe accounts for a quarter of all lung cancer deaths globally despiterepresenting an eighth of the world’s population [2]. Recent advances in techniques for diagnosis, stagingand treatment have seen a modest improvement in outcomes and there is hope that further developmentsin molecular targeted treatments and immunotherapy, as well as potential combination treatments andthe expected implementation of low radiation dose computed tomography (CT) screening, will furtherimprove outcomes [3]. However, improvements in clinical services vary greatly across Europe owing to avariety of organisational, economic and sociopolitical factors. To help drive the adoption of best clinicalpractice that is delivered more equitably, an agreed service specification and agreement on the metrics bywhich the service can be measured are needed. This requires a description of the standards for lung cancerservices and a uniform cancer registration system to measure the activity.
In 2015, the European Respiratory Society (ERS) approved a task force to create a pan-European thoraciconcology dataset and develop internationally agreed standards for European thoracic oncology centres.The membership of the task force was derived from a previously successful task force on qualitymanagement in lung cancer and hence includes a multidisciplinary group with a keen interest in thedevelopment of harmonised international standards. The two main aims of this group were to develop apan-European dataset and a manual of standards for lung cancer services in Europe.
Lung cancer registration in Europe: the need for a pan-European datasetCancer data collection in Europe began in the 1950s with the establishment of cancer registries. However,it was not until the 1990s that they were widespread enough to allow meaningful comparative research tobe done. The EUROCARE series of large-scale publications demonstrated the variation in epidemiologicalfeatures and outcomes in a large number of European countries [4, 5]. These publications have sparkedinterest from the public and politicians alike, and they have been the catalyst for many developments atthe national and international level to improve outcomes for individuals with cancer. The number ofcancer registries involved in EUROCARE studies has grown, and the level of population coverageimproved, but there remain large parts of Europe that are not accounted for in these studies [6]. Dataitems and their definitions are not universally agreed, and so comparisons cannot always be standardised.Furthermore, few registries collect sufficient clinical details at the individual patient level to supportmeaningful comparisons of outcome within and between countries.
The strategy of the European Union (EU) against cancer has focused on the importance of cancerregistration. The EU has funded several initiatives, including the European Action Against CancerProgramme (1985–2008), the European Partnership for Action Against Cancer (EPAAC) (2009–2014) [7]and the EU Cancer Control Joint Action (CANCON) [8]. The European Network of Cancer Registries(ENCR) was set up in 1990 as a joint venture with several other international cancer research groups topromote the quality of cancer registration across Europe and the use of these data for clinical and public
health research. The ENCR has published a minimum dataset for cancer registries as well as an optionaldataset [9]. These are generic for every cancer rather than being lung cancer specific.
Lung cancer services in Europe: the need for harmonised international standardsEurope has a diverse healthcare structure generated by diversity in social, political and economic factors.However, in thoracic oncology, the aim of the healthcare system is to provide the best standard of care toprovide patients with the best outcomes. In general, countries have a combination of large centres, usuallybased in large hospitals with a concentration of expertise and technology, and smaller healthcareproviders, with less equipment and less comprehensive services. Some countries have additional primarycare services that play a crucial role throughout the lung cancer pathway. A previous ERS task force reportdescribed the differences in the healthcare infrastructure for 38 European countries [10]. The diversityacross Europe has undoubtedly contributed to the variation in healthcare outcomes, and agreement on thestandards that centres should adopt is one way to mitigate this effect.
MethodsGroup compositionThe task force was chaired by Anna Rich and Torsten Blum with a further 25 members from ninecountries around Europe. All members have a specialist interest in lung cancer, and represent differentaspects of the multidisciplinary team (MDT): pathology, pulmonology, radiation oncology, medicaloncology, thoracic surgery, palliative care, a lung cancer nurse specialist (LCNS) and a medical statistician.Patients’ views were represented through the lung cancer patient advisory group (PAG) of the EuropeanLung Foundation (ELF).
Conflicts of interestAll task force members declared and signed conflict of interest statements at the beginning of the projectand updated them at project finalisation.
Working methodsThe task force met at face-to-face meetings held at the ERS congress in Amsterdam in September 2015.The aims and objectives of the project were discussed and agreed, and the proposal for two work streams,led by Anna Rich (minimum dataset) and Torsten Blum (manual for lung cancer services), was ratified.Further face-to-face meetings were held in London in May 2016, at the ERS congress in London inSeptember 2016 and in London in March 2017. A final face-to-face meeting was held at the congress inMilan in September 2017 when the final report was discussed in detail. Conference calls and e-mailcorrespondence were also used to discuss and amend details within the minimum dataset and the manualof lung cancer services as they were developed.
Review of existing datasetsDatasets in use or in development were reviewed before and during meetings of the task force. Theseincluded the work from an allied project [11] as well as national datasets from countries represented on thetask force. Supplement 1.1 reports the datasets reviewed and key facts regarding their development. Theaim was to understand the similarities and differences in data collected and to derive a harmonised datasetthat would encompass, as far as possible, existing data collected, as well as extending to a minimum dataset.Existing datasets from ENCR and the International Consortium for Health Outcome Measures (ICHOM)were used as reference datasets [9, 12]. These were chosen for their comprehensiveness and because theywere developed by international groups. However, the task force identified these datasets as being toodetailed and ambitious to be applied as harmonised standards in Europe, where a more pragmaticapproach is needed.
Membership of the task force included professionals who have considerable experience in developing andimplementing national audits. This expertise was used to make realistic proposals for a European dataset.The data items were chosen on the basis of consensus opinion, with a majority of >90% agreement.
Evidence search and review of existing manualsMembers of the task force performed a narrative search of existing manuals for lung cancer services. Thissearch included relevant websites or printed publications of related international societies and otherstakeholders, and national-level publications accessible to task force members (supplement 1.2). Given thata systematic search on the national level was beyond the means of this task force, the group accepteda potential selection bias based on a limitation to only those European countries represented on thetask force.
During the course of this task force, Torsten Blum browsed repeatedly through the websites of the namedinternational societies and other stakeholders for substantial online or referenced printed publications. Evidenceretrieved from this narrative search as well as from reports identified by other task force members wasamalgamated (by T. Blum) and then discussed during task force meetings. All searches on the internationallevel were last updated in November 2017 (by T. Blum). Detailed results are provided in supplement 1.2.
The previous ERS task force on quality management in lung cancer care revealed that there are more than150 lung cancer guidelines worldwide, and more than 80 within Europe [10]. There was significantvariation in the quality of these guidelines, in terms of the underlying evidence used, the specific aspectsof the lung cancer pathway being addressed and the publication date. Only a minority of these guidelinesaddressed the infrastructure and pathway processes in any meaningful way that would allow them toinform our aspired manual of standards for lung cancer services.
The task force did not perform systematic evidence searches in medical databases on its own, but usedrelevant results from a Grading of Recommendations Assessment, Development and Evaluation(GRADE)-based systematic review of the literature on quality management in lung cancer with a focus onthe impact of defined lung cancer services. This was the subject of a parallel ERS task force that will bepublished in full separately. Overall, published material was found to be very limited and of low quality.
An agreed list of standards for lung cancer services in Europe was developed during task force meetingsand interim discussion. The recommended manual of standards for lung cancer services is based on areview of available evidence and is complemented by the inclusion of patient perspectives as well as theclinical experience of the task force members.
The European Lung Foundation patient advisory groupThe ELF lung cancer PAG was established to support a range of research activities relating to lung cancer.The PAG is made up of people who have received a diagnosis of lung cancer (either undergoing treatmentor survivors), caregivers of people with lung cancer and representatives of lung cancer patientorganisations. Every member responded to an advert on the ELF website and was interviewed informallyby phone or Skype before being accepted onto the PAG. The PAG allows individuals to self-select whichprojects they can most usefully support, based on their experience and interests, and also allows them towithdraw at any time if health issues arise.
The task force considered it essential that the dataset and manual created be meaningful to patients. ELFstaff member Jeanette Boyd was invited to attend task force meetings and facilitate the gathering of viewsfrom PAG members regarding the development of both the pan-European dataset and the manual forlung cancer services. Five members provided feedback on the dataset (four patients and one patientorganisation representative; from Czech Republic, Italy and UK) and four members provided feedback onthe manual of lung cancer services (two patients, one caregiver and one patient organisationrepresentative; from Denmark, Ireland, Poland and the UK). Views were gathered by sharingdocumentation via email and requesting feedback. Jeanette Boyd collated and analysed the feedback usinga qualitative approach and presented this to the task force for consideration. In addition, Torsten Blumconducted semi-structured telephone interviews with PAG members for feedback relating to the manual oflung cancer services.
Manuscript preparationAnna Rich and Torsten Blum wrote the task force final report, with editing and some modificationprovided by David Baldwin. Michael Peake was invited to write the subsection regarding the NationalLung Cancer Audit of England and Wales, as an external co-author. The paper was then circulated to allmembers of the task force and revisions made by Anna Rich. The statement paper and supplements werereviewed, edited and approved by all members of the task force before submission.
Part 1. Development of a pan-European lung cancer datasetTwo national lung cancer datasets stood out as exemplars of data completeness and the use of data todrive improvement in services and outcomes; they are described below.
Drivers, development and implementation of two national lung cancer audit programmes:Denmark and EnglandDriversThe two main drivers behind the development of both of these well-established audit programmes were 1)preliminary comparative data in the 1990s suggesting poorer outcomes than in other countries and 2)evidence for unwarranted variation in clinical practice. EUROCARE-1 reported 5-year survival in lungcancer in England and Denmark as being <8% [4]. This prompted the Royal College of Physicians of
London, with funds provided by the English Government, to sponsor a snapshot audit [13]. This audit,involving 52 hospitals between 1995 and 1996, showed large variations in the care of lung cancer patientsand led to efforts to establish a longer term, population-based lung cancer audit programme. In Denmark,similar variations were apparent. The healthcare system was organised so that diagnostics and treatmentwas provided by a large number of hospital departments with very different approaches to the disease. TheDanish Lung Cancer Group (DLCG) was formed with the primary aim of improving the clinicalmanagement and survival of Danish lung cancer patients. A secondary aim was to produce a platform forlung cancer research. The DLCG produced national guidelines for the management of lung cancer [14]and adopted a strategy to implement the guidelines and concurrently monitor the implementation byreporting to a national registry, known as The Danish Lung Cancer Registry (DLCR).
Development and implementationThe Danish Lung Cancer RegistryThe DLCR started in 2000 and now contains data on ∼70000 patients. Between 2000 and 2012, inclusionof patients relied on clinicians identifying and reporting patients to the DLCR, but since 2013 patientshave been identified from the first diagnostic codes for lung cancer in the Danish National Patient Registry(DNPR). The latter helped improve data completeness and reduce the workload for clinicians.Participation has since become mandatory by law, so data completeness is now >95% of new cases. Thebasic database is derived from the DNPR and the Danish Pathology Register and includes procedures andtreatment. This is supplemented and validated online by clinicians to form the DLCR. All departmentsinvolved in the diagnosis and treatment of lung cancer in Denmark are responsible for the validation andsupplementation of data [15].
The database contains demographic and patient characteristics and details of treatment, including surgery,type and duration of chemotherapy, and type and duration of radiation. Patients’ vital statuses are derivedmonthly from the Danish Civil Registration System and age at diagnosis confirmed from the personalidentification number. During the 18 years of data collection in the DLCR, major improvements intreatment outcomes have been recorded [16]. The DLCR has developed a number of indicators usingscientific evidence and the national guideline recommendation. The indicators are reported monthly andannually to all participating departments, hospitals and healthcare authorities. A comprehensive system ofaudits ensures that differences in quality measures and failure to meet standards are evaluated.
A number of publications based on the DLCR have appeared since 2009, documenting the effects of anational registry. The two major lessons that have been learned are first that high data quality andcompleteness is essential to ensure that clinicians will work with the data and results from the database.Meaningful audit depends on the accuracy and credibility of data; only once clinicians are convinced ofthis is it possible to shift the focus from data quality to the findings. Second, it is important that hospitaland regional management are involved in the implementation process to facilitate the changes in servicesand clinical practice that are recommended by the findings of the audit [17]. Centralisation in Denmark istraditionally met with resistance from local stakeholders, and the involvement of management has played acentral role. The DLCR has shown that regional differences have decreased as the number of departmentsinvolved in treating lung cancer patients has halved [17].
In 2017, the DLCG formulated an ambitious goal to double survival from lung cancer before 2030 [18]and it is widely recognised that the DLCR plays a crucial part in achieving this goal.
The National Lung Cancer Audit (UK)In 1999, a multidisciplinary “intercollegiate” lung cancer group published: “Lung Cancer: a Core Dataset”[19]. From the outset, the aim was to achieve as near to total population coverage as possible; in order tomake achieving this more likely, the size of the dataset was limited. It has evolved over the years [20], butthe number of fields requiring completion for any one patient is usually less than 50.
In 2004 the English Government, through the National Clinical and Patient Outcomes Programme, whichfunds over 30 national clinical audits in England, began to support the central functions of a national lungcancer audit (NLCA) programme. Wales joined the programme in 2006, and collated data from Scotlandand Northern Ireland have been included in reports whenever possible.
The principles of the NLCA and findings were regularly presented at regional and nationalmulti-professional clinical meetings to encourage clinical engagement, which was initially limited.However, despite non-mandatory participation, the proportion of patients captured by the audit rose from40% in 2005 to 100% in 2009 and has remained at that level since. In 2009 participation was mandated byformal contract between the Department of Health and provider hospitals.
https://doi.org/10.1183/13993003.00610-2018 5
ERS STATEMENT | A.L. RICH ET AL.
A bespoke database was developed (Lung Cancer Data (LUCADA)) in one of the central computingsystems of the National Health Service (NHS), allowing direct, secure entry of individual patient data orcompiled grouped data on multiple patients as .csv or .xml formatted files. This system also allows eachhospital to see its own grouped data at any time with comparative, anonymised data from other hospitals.
MDTs were already well established [21] and these teams were used as the focus for data collection, withsome teams appointing data coordinators or building the work into the roles of MDT coordinators or evenLCNSs. Each local hospital developed or purchased its own software for data collection, though by the late2000s >80% were using one of two systems. Data completeness improved rapidly, e.g. completeness ofperformance status and stage data fields reached >80% by 2009 [22] and have exceeded 90% since [23].
The first annual report of the NLCA was published and made available to the general public in 2006 [24].The hospitals were identified along with their activity, data completeness and outcomes. This led to a greatdeal of press activity and complaints from hospitals that their data were not accurate, but this served as avital driver behind the rapid improvements in participation and data completeness that followed. Reportsand anonymised spreadsheets of data are now available to the public via the Royal College of Physicians’website [25].
Data quality and completeness are major issues for any large-scale population-based audit. Data oncomorbidity proved to be difficult to collect, being both incomplete and inconsistent. As with the DLCR,the Charlson index is used, derived from inpatient diagnostic codes. Until recently, detailed data oncombination therapies and second and subsequent lines of treatment have been limited; this is nowcollected through two other databases, one for radiotherapy and one for systemic therapy. Palliative care,primary care and patient-reported outcome measures have so far not been routinely linked to the NLCA.
The NLCA has changed the culture of the thoracic oncology community in the UK, raising awareness oflocal and regional activity, patterns of care, and outcomes of patients with lung cancer and mesothelioma.Surgical resection rates have doubled since the audit began and less dramatic improvements have beenseen in a wide range of other indicators of high-quality care [25]. The 1- and 5-year survival rates haveincreased in recent years [26] and appear to parallel the improvements in treatment rates. A large numberof peer-reviewed publications have emerged using the NLCA data and these have been influential inrecommendations for the commissioning of services. In 2014 the NLCA team at the Royal College ofPhysicians began working directly with the National Cancer Registration and Analysis Service (NCRAS) inPublic Health England and to a large extent now use data collected in the national Cancer Outcomes andServices Dataset (COSD) as the basis of their analyses and reports.
Patient perspectives on the development of a pan-European lung cancer datasetThe ELF lung cancer PAG was asked specific questions about the development of a pan-European datasetand the views outlined below are from five individuals with experience of lung cancer from the CzechRepublic, Italy and the UK.
Value of a pan-European datasetPAG members were in agreement that the implementation of a lung cancer dataset across Europe wouldbe particularly useful in:
• developing and monitoring diagnostic standards;• developing and monitoring standards of care in lung cancer;• assisting evidence-based analysis of data across countries; and• establishing what treatments work and for whom.
Patient access to data would be of interest and value to patients as a way to understand more about theircondition and what could be viewed as usual or unusual in comparison with others. This would giveindividuals a useful comparator to discuss their condition with clinicians. In light of this, patient access tothe data should be considered as part of any dataset development.
Gathering dataIt was noted that patients could provide valuable input in defining the relevant importance of differentquality of life (QoL) data and the considerations to be aware of when collecting these data. Patients felt itwas important for QoL data to be collected verbally, directly from patients, to ensure consistency, and toidentify patterns across the pathway which could then lead to the identification of relevant support whereappropriate. A crucial factor for the successful gathering of information from the patient is the level oftrust that exists between clinician and patient. The task force identified the QoL questionnaire from theEuropean Organization for Research and Treatment of Cancer (EORTC QLQ-C30) as a possible resource
https://doi.org/10.1183/13993003.00610-2018 6
ERS STATEMENT | A.L. RICH ET AL.
because this is a standardised tool in current use [27]. The PAG members thought that some of thequestions were relevant, but that a subset of these questions might be more effective.
PAG members suggested that there could be a beneficial role for caregivers, nurses and hospice staff in helpingto gather QoL information and assisting patients, especially at times of high stress and anxiety. They identifiedthese times as often being at the point of diagnosis; when patients may not have much energy, e.g. duringchemotherapy; or when receiving palliative care. This will vary with each individual and further discussionswould be beneficial to ensure data are both sensitively and effectively gathered. Patient-reported outcomeshave demonstrated positive impact on treatment outcomes and their use is expected to increase in the future[28]. Specific recommendations on patient-reported outcomes are not dealt with in this recommendation.
The PAG thought QoL data collection would be most valuable at diagnosis, post primary treatment(3 months) and at the end of primary treatment (6 months). Several PAG members felt that it would behelpful to gather data after 12 months. It was also suggested that collecting QoL from patients at the endof a 5-year recurrence-free follow-up could be valuable in sharing hope among patients.
PAG members recommended that the gathering of comorbidity data should be patient led and clinicianreported. These data should emerge from discussion and agreement between the clinician and patient.This would have the additional advantage of patients being better informed about potential comorbiditiesand provide opportunities for pre-agreement with their clinician about what to do should symptomsappear, potentially leading to lower patient anxiety in the long term.
Implementation topics of importance to patientsImplementation topics identified as important to patients included informed patient consent, dataprotection and data security, data use and patient knowledge of how it is used, and information aboutclinical trial involvement. Providing personalised data summaries with pan-European comparisons wouldalso be a valued option.
ELF would recommend that patient representatives are fully involved in future discussions about datasetdevelopment to ensure that all patient issues have been considered and any potential challenges addressedbefore any future roll-out across Europe.
Recommendations for a pan-European dataset for lung cancer registrationThe proposed pan-European dataset for lung cancer registration can be divided into four sections, withdata items relating to basic patient features, tumour details, extended patient features and details of thelung cancer pathway and process (tables 1–4; these tables are available as a separate download assupplement 2). The tables include data items that should be mandatory in the minimum dataset (markedin black in supplement 2) as well those which are desirable (marked in blue in supplement 2). Data itemsin the minimum dataset were felt to be essential for the basic epidemiology required to evaluate keyclinical outcome measures, and are already collected in a majority of European countries [11]. Theminimum dataset for lung cancer (including tracheal cancer) is for all patients with an InternationalClassification of Disease version 10 code of c33 or c34.
Basic patient featuresTable 1 illustrates data items for basic patient features. A record of ethnicity is important for severalreasons. There is evidence of significant variations in the prevalence of somatic mutations inadenocarcinoma of the lung based on ethnicity [29, 30]. There is also evidence of variation in the route toaccessing healthcare services based on patient ethnicity [31–33]. However, it is difficult to find one codingsystem for ethnicity that would capture the needs of every country in Europe. The ICHOM datasetdefinition [12] states that individual countries should determine the definition, and therefore this data itemis not suitable for cross-country comparison. The task force therefore concluded that it was not possible topropose one list of ethnicity codes that would be relevant for every country in Europe (an example of acoding system is shown in supplement 1.3). The educational level of an individual was chosen as asurrogate for socioeconomic status. Some countries have well-established linkage between registries orindependent lung cancer audit programmes and census data which allow them to stratify an individual’ssocioeconomic status. However, these are in the minority, and although socioeconomic status is a veryimportant indicator of access to healthcare generally, as well as key clinical outcomes in thoracic oncology[34–36], a compromise was agreed. The task force adopted a simple outline of educational level achievedbased on ICHOM (primary, secondary or tertiary) [12]. There is wide variation in the level of educationalstatus achieved in different countries, and it is not an ideal surrogate for socioeconomic status, but despitethis limitation it was thought that educational level would be a data item that could be captured.
Five data items relate to the diagnosis of lung cancer, i.e. how it was made, with the inclusion of pertinentdates; these will be powerful points of reference when interpreting the lung cancer pathway and processes
within each country or between countries. Delays in referral to a lung cancer specialist have been proposedas a reason for differences in outcomes, so the date of referral to a lung cancer specialist is included. Theroute to a lung cancer specialist varies across Europe, and it often does not involve a primary care physician[10]. There is a hierarchical basis to the date of diagnosis, which is taken from the ENCR minimum
TABLE 1 Basic patient features
Data item Definition Detailed definition
Date of birth dd/mm/yyyy
Sex Male or female 1=male2=female999=undisclosed/unknown
Date of referral dd/mm/yyyy Date on which referral made with respect to potential lung cancer. This could includeself-referral, primary to secondary care, within secondary care.
Option for missing/unknown.
Date of diagnosis dd/mm/yyyy Date the first histopathology/cytology sample was taken which confirmed malignancy.If date of histopathology sample not available then index date based on followingcriteria in descending order (as per IARC):
1) Date of first histological or cytological confirmation of this malignancy (with theexception of histology or cytology at autopsy). The date should be provided in thefollowing order of preference:
i) date when the specimen was taken (biopsy)ii) date of receipt by pathologistiii) date of the pathology report.
2) Date of admission to hospital because of this malignancy.3) When evaluated at an outpatient clinic only: date of first consultation at the
outpatient clinic because of this malignancy.4) Date of diagnosis other than 1, 2 or 3.5) Date of death, if no information is available other than the fact that the patient died
of a malignancy.6) Date of death, if the malignancy is discovered at autopsy.
Date of final pathologyreport
dd/mm/yyyy Date of final pathology report to include molecular analysis where appropriate.Option for missing/unknown.
Mode of presentation How was lung cancerfirst suspected?
Numerical code
0=screening1=symptoms2=incidental finding3=other (free text box to specify)999=don't know
Basis of diagnosis Numerical code (ICHOM) 1=clinical2=histology3=cytology999=unknown
Clinical Diagnosis made before death with or without diagnostic techniques (e.g. chestradiography, endoscopy, imaging, ultrasound, exploratory surgery) but without atissue diagnosis.
Histology Histological examination of tissue from the primary tumour or metastasis, including allcutting and bone marrow biopsies. Also includes autopsy specimens.
Cytology Examination of cells whether from a primary or secondary site, including fluidsaspirated using endoscopes or needles. Also including microscopic examination ofperipheral blood films and trephine bone marrow aspirates.
Data items in roman are mandatory within the proposed minimum dataset; data items in italics are desirable within the dataset. dd/mm/yyyy:date, month, year; ICHOM: International Consortium for Health Outcome Measures; IARC: International Agency for Research on Cancer.
https://doi.org/10.1183/13993003.00610-2018 8
ERS STATEMENT | A.L. RICH ET AL.
dataset for cancer registries [9]. The date of the final pathology report reflects the need to identify delaysin obtaining a complete pathological diagnosis that are consequent upon increasingly complex processing.The mode of presentation is an essential data item because it is known to influence prognosis.
The basis of diagnosis (clinical/radiological or pathological) is crucial because of the association withprognosis: a more precise identification of the denominator for the whole cohort allows internationalcomparisons to reduce selection bias. Comparisons must use the same denominator because cohorts thatonly include patients with pathological confirmation do not include those patients with an often worseprognosis, who are diagnosed purely on the basis of a high level of clinical suspicion; such patients are oftentoo unwell or too frail to undergo further tests. There is evidence that the likelihood of obtaining pathologicalconfirmation in individuals believed to have lung cancer is affected by several factors. These include age [37],socioeconomic status [38] and performance status (PS) [39]. Equally, factors relating to the lung cancerservice could account for variation in pathological confirmation rates, and hence the recommendation foragreed standards among lung cancer services in Europe (see “Part 2. Manual of standards for lung cancerservices in Europe”). Internationally there is no agreed pathological confirmation rate, but the NLCA ofEngland found that higher pathological confirmation rates were most strongly associated with survival inpatients with stage I/II disease who had a PS of 0–1 [40]. Thus, a stratified approach to pathologicalconfirmation based on clinical features was suggested, rather than a single benchmark figure forpathological confirmation rate. The basis of diagnosis is the same as that defined by ICHOM [12].
Tumour detailsData that specify details of the tumour (table 2) are essential for international comparisons because of thestrong influence on prognosis, type of treatment offered and prediction of treatment response. Thepathological subtype is vital, and we know that different countries within Europe use different systems.The majority use the International Classification of Diseases for Oncology, 3rd edition, which incorporatesall subtypes according to the current 2015 World Health Organization classification of lung tumors [41],including the new lung adenocarcinoma classification originally proposed by the International Associationfor the Study of Lung Cancer (IASLC), American Thoracic Society and ERS [42]. However, Denmark usesSystematized Nomenclature of Medicine (SNOMED). The task force recommends that data are enteredinto the system using whichever classification is standard practice within each country. Retrieval of specificpathological subtypes could then be reconstructed with automated algorithms. For those countries withouta specific pathological classification system, we have created a small but clinically relevant list ofpathological subtypes. The field of molecular analysis is expected to expand in the future and so the datacollection system needs to be able to include new definitions as clinical practice changes. These changescould be incorporated during a revision programme every 2 years, in order to balance clinical developmentwith practical utility.
Stage of disease at diagnosis is compliant with the IASLC staging system [43]. The basis of the stagereflects access to certain procedures as well as national guidelines for diagnosing lung cancer, so there aredata fields to record which investigations have been performed prior to the formation of a “finalpretreatment clinical stage”. The version of the staging system (7th or 8th edition) is selected first, andthen the individual T, N and M stage is entered. Further details about tumour size and the number andlocation of nodes and metastases then follow. Sub-classification of the extent of N2 disease is included aspart of the desirable dataset, which could then be used to categorise the patient cohort based on either theRobinson classification [44] or the IASLC staging project (assuming N1 disease is also sub-classified;table 2) [45]. This level of detail from a pan-European cohort of individuals with lung cancer will allow fora comprehensive and very detailed analysis of the prognostic value of the current IASLC staging system.
Extended patient featuresTable 3 captures the extended patient features. The main data item in this section is the PS of theindividual at the time of diagnosis with lung cancer. The Eastern Cooperative Oncology Group (ECOG)system [46] (also known as the World Health Organization PS) is the most widely used method forrecording this feature, although there is evidence that PS is only routinely collected in less than a third ofEuropean countries [11]. It is paramount that collecting this patient feature becomes routine in allregistries or audit programmes given the important role PS plays in predicting outcome [39, 47–50].
The subsequent data items would allow a detailed evaluation of the clinical outcomes from lung cancerwithin and between countries. The majority of European countries do not collect many of these items, andit would take significant investment and political support to achieve this. Assessing comorbidities is afundamental part of patient evaluation prior to making a treatment plan, and there is good evidence forthe influence of comorbidity on outcome [51–54]. The Charlson index was developed in the late 1970sand validated on a cohort of patients with breast cancer [55]. It has subsequently been used in numerous
https://doi.org/10.1183/13993003.00610-2018 9
ERS STATEMENT | A.L. RICH ET AL.
TABLE 2 Tumour details
Data item Definition Detailed definition
Histology System used ICD-O-3 (covers the entire 2015 WHO Classification of Tumours ofthe Lung, Pleura, Thymus and Heart)
SNOMEDBased on which system is used, a list of possible options willappear, and the correct histology field can be ticked.
If no recognised system used then drop-down menu appears with a limited list:1=small cell carcinoma2=NSCLC NOS3=squamous cell carcinoma4=adenocarcinoma5=large cell neuroendocrine carcinoma6=carcinoid-typical7=carcinoid-atypical8=adenocarcinoma in situ9=spindle/pleiomorphic/giant cell NSCLC10=other (free text box appears)999=unknown
Molecular analysis# Was this performed?Numerical code
0=no1=yes999=don't know
Further questions only relevant ifmolecular analysis performed
EGFR mutation(ICHOM)
Numerical code
Indicate presence of EGFR activating mutation0=no1=yes2=failed analysis999=don't know
Indicate presence of RET translocation0=no1=yes2=failed analysis999=don't know
METNumerical code
Indicate presence of MET amplification0=no1=yes2=failed analysis999=don't know
MET exon 14Numerical code
Indicate presence of MET mutation exon 140=no1=yes2=failed analysis999=don't know
HER 2Numerical code
Indicate presence of HER2 mutation0=no1=yes2=failed analysis999=don't know
Stage Final pretreatment clinical stageBasis of stage What method was used to decide the
final pretreatment clinical stage?Numerical code
0=imaging only1=imaging AND non-surgical pathology samples¶
2=imaging and surgical biopsies (mediastinoscopy, VATSprocedure)
999=don't know
Investigations performed? CT scanNumerical code
0=no1=yes999=don't know
PET-CTNumerical code
0=no1=yes999=don't know
BronchoscopyNumerical code
0=no1=yes999=don't know
EBUSNumerical code
0=no1=yes999=don't know
EUSNumerical code
0=no1=yes999=don't know
MediastinoscopyNumerical code
0=no1=yes999=don't know
Histopathology or cytology from nodeoutside chest
Numerical code
0=no1=yes999=don't know
Sampling of pleura or pleural fluidaspiration (medical)
Numerical code
0=no1=yes999=don't know
VATS thoracoscopyNumerical code
0=no1=yes999=don't know
Imaging of metastasis (e.g. CT/MRIbrain, MRI spine, MRI adrenal)
Numerical code
0=no1=yes999=don't know
Histopathology of metastasis(e.g. liver biopsy)
Numerical code
0=no1=yes999=don't know
Continued
https://doi.org/10.1183/13993003.00610-2018 11
ERS STATEMENT | A.L. RICH ET AL.
studies, but it has limited functionality given the complexity of the score, the lack of clarity regardingseverity of comorbid disease and the out-of-date weighting given to HIV/AIDS. The Adult ComorbidityEvaluation-27 (ACE-27) score is an alternative model used by some to quantify comorbid disease [56],and some countries record specific comorbid diseases, but the list is variable [11]. Therefore, the ICHOM
TABLE 2 Continued
Data item Definition Detailed definition
Exploratory open thoracic surgeryNumerical code
0=no1=yes999=don't know
Tumour size Numerical value The longest single direction size in cm to one decimal point (e.g. 3.2)
Staging system Which staging system has been used? IASLC 7th or 8th editionBased on this answer; drop-down menu appears for T, N andM stage.
Tumour stage Mixed value IASLC 7th edition; 1a through to 4IASLC 8th edition; 1mi through to 4999=unknown/X
Nodal stage Mixed value IASLC 7th or 8th edition; 0 through to 3999=unknown
Extent of N1 disease Numerical code 0=not applicable1=single station N1 disease2=multi-station N1 disease
Extent of N2 disease Numerical code 0=not applicable1=microscopic N2 node found at final pathological (post-operative)specimen
2=single station N2 node without N1 disease (‘skip’ lesion)3=single station N2 node with N1 involvement4=multi-station N2 disease5=bulky or fixed multi-station N2 disease
Metastasis stage Mixed value IASLC 7th edition: 0 through to 1bIASLC 8th edition: 0 through to 1c999=unknown/X
Number of metastatic lesions Numerical value 0=no metastatic spread (i.e. M0 above)1, 2, 3 onwards999=don't know
Site of metastases LiverNumerical code
0=no1=yesIf yes, specify number of metastatic lesions 1, 2, 3 onwards999=don't know
BrainNumerical code
0=no1=yesIf yes, number of metastatic lesions 1, 2, 3 onwards999=don't know
AdrenalNumerical code
0=no1=yesIf yes, specify number of metastatic lesions 1, 2, 3 onwards999=don't know
BoneNumerical code
0=no1=yesIf yes, specify number of metastatic lesions 1, 2, 3 onwards999=don't know
Other Free text box to confirm site of spread
Data items in roman are mandatory within the proposed minimum dataset; data items in italics are desirable within the dataset. ICD-O-3:International Classification of Diseases - Oncology, 3rd edition; WHO: World Health Organization; SNOMED: Systematized Nomenclature ofMedicine; NSCLC NOS: non-small cell lung cancer not otherwise specified; VATS: video-assisted thoracic surgery; EBUS: endobronchialultrasound; EUS: endoscopic ultrasound; CT: computed tomography; PET: positron emission tomography; MRI: magnetic resonance imaging;IASLC: International Association for the Study of Lung Cancer; T: tumour; N: node; M: metastasis. #: annual updates expected as molecularmedicine develops; ¶: definition of non-surgical samples: EBUS, EUS, percutaneous lung or pleural biopsy, pleural aspiration, bronchoscopy.
https://doi.org/10.1183/13993003.00610-2018 12
ERS STATEMENT | A.L. RICH ET AL.
list of comorbid diseases (based on SANGHA et al. [57]) is recommended, but should be derived from themedical notes after consultation between the clinician and the patient. It is hoped this will ensure accuraterecording of all known comorbidities. The EORTC QLQ-C30 patient-completed questionnaire isrecommended for QoL [27]. This is based on the fact it is a validated research tool [58], although our
TABLE 3 Extended patient features
Data item Definition Detailed definition
Performance status (finalpretreatment)
ECOG (WHO)Numerical code
0=Able to carry out all normal activity without restriction.1=Restricted in physically strenuous activity, but able to walk and dolight work.
2=Able to walk and capable of all self-care, but unable to carry outany work. Up and about more than 50% of waking hours.
3=Capable of only limited self-care, confined to bed or chair morethan 50% of waking hours.
4=Completely disabled. Cannot carry on any self-care. Totallyconfined to bed or chair.
999=Unknown/not recorded
Smoking status Numerical code (ICHOM) 1=never smoker (<100 cigarettes ever)2=ex-smoker (stopped at least 1 year before inclusion, i.e. diagnosis)3=current smoker999=don't know
Smoking pack-years Numerical value The number of pack years smoked, regardless of ex or current smokerstatus (e.g. 20, 40)
999=don't know
Comorbidity at baseline frommedical consultation with patient
Have you been told by a doctor that you have any of the following:0=I have no other diseases1=heart disease (e.g. angina, heart attack or heart failure)2=high blood pressure3=leg pain when walking due to poor circulation4=lung disease (e.g. asthma, chronic bronchitis, COPD or emphysema)5=diabetes6=kidney disease7=liver disease8=problems caused by stroke9=disease of the nervous system (e.g. Parkinson disease, multiplesclerosis)
10=other cancer (within the last 5 years)11=depression12=arthritis
Weight Numerical value In kg999=don't know
Height Numerical value In m999=don't know
Lung function (at baseline) Numerical value (ICHOM) Observed FEV1 in L (e.g. 1.35)999=don't know
Numerical value (ICHOM) FEV1 % pred (e.g. 56 would represent 56% predicted)999=don't know
Numerical value Observed FVC in L (e.g. 2.3)999=don't know
Numerical value KCO % pred (e.g. 85 would represent 85% predicted)999=don't know
Quality of lifeAt diagnosis EORTC QLQ-C30 Score (maximum value 126)At end of first-line treatment EORTC QLQ-C30 Score (maximum value 126)At 6 months post-diagnosis EORTC QLQ-C30 Score (maximum value 126)
Data items in roman are mandatory within the proposed minimum dataset; data items in italics are desirable within the dataset. ECOG: EasternCooperative Oncology Group; WHO: World Heath Organization; ICHOM: International Consortium for Health Outcome Measures; COPD: chronicobstructive pulmonary disease; FEV1: forced expiratory volume in 1 s; FVC: forced vital capacity; KCO: transfer coefficient of the lung for carbonmonoxide; EORTC QLQ: European Organization for Research and Treatment of Cancer Quality of Life Questionnaire.
https://doi.org/10.1183/13993003.00610-2018 13
ERS STATEMENT | A.L. RICH ET AL.
TABLE 4 Lung cancer outcomes
Data item Definition Detailed definition
Contact made with LCNS Numerical code 0=no1=yes999=don't know
Treatment intent(reflects the intent of thetreating physician or MDT)
Numerical code 1=curative intent2=non-curative intent3=no active treatment999=don't know
Curative This is single or multimodality treatment which is hoped willremove the threat of lung cancer to the patient's lifeexpectancy.
Non-curative This is single or multimodality treatment which is expected togain local control, or limit the progression of the disease,but is unlikely to remove the threat of lung cancer to thepatient's life expectancy.
No active treatment For those patients who decline, or are too frail for,radiotherapy or chemotherapy and receive medication forsymptom control or a watch and wait policy.
First-line treatment given toprimary tumour
Numerical code Choose one option only from the list below:1=surgery alone2=hyperfractionated radiotherapy3=external beam radiotherapy (curative intent but not CHART)4=stereotactic radiotherapy5=radiofrequency/microwave ablation6=brachytherapy7=palliative radiotherapy to lung primary8=concurrent chemoradiotherapy9=sequential chemoradiotherapy10=induction radiotherapy (pre-surgery)11=induction chemotherapy (pre-surgery)12=palliative chemotherapy13=targeted/biological therapy (TKI etc.)14=immunotherapy15=interventional bronchoscopy16=specialist palliative care17=other (free text)999=don't know/not recorded
First-line treatment not given orchange in treatment plan
Numerical code 0=not relevant1=patient declined first-line treatment offered2=patient deteriorated and no longer eligible for first-linetreatment
3=hospital unable to provide first-line treatment4=other (free text)
Date of first-line treatment dd/mm/yyyy Date of the start of first-line treatment, i.e. date of operation,first day of radiotherapy or chemotherapy regime, orappointment with specialist palliative care physician.
Type of operationAdditional question only ifoption 1 above
Numerical code 0=no1=yesIf yes, then further question appears
Type of additional supportivefirst-line treatment
Numerical code 1=stereotactic radiotherapy to brain metastases2=radiotherapy for spinal cord compression3=prophylactic cranial irradiation4=whole brain radiotherapy5=radiotherapy for oligometastases6=SABR for oligometastases7=radiotherapy for SVCO8=radiotherapy to mediastinum9=specialist palliative care10=surgical resection of metastases11=pleural intervention (see below)12=other (free text)
Date of first radiotherapy session dd/mm/yyyy
Nature of radiotherapy (1–8 above) Total dose given (Grey) Absolute number (e.g. 30)Number of fractions Absolute number (e.g. 6)Number of days or radiotherapy
treatmentAbsolute number (e.g. 12)
Date of palliative care dd/mm/yyyy Date of first appointment with specialist palliative care physician
Date of surgery dd/mm/yyyy
Date of pleural intervention dd/mm/yyyy
Type of pleural intervention Numerical code 1=thoracocentesis2=chest drain3=pleurodesis4=indwelling chest drain
How is the patient followed up afterfirst-line treatment?
Numerical code. Pick single item fromlist.
Options are ranked in descending order.If multiple answers apply, pick the firstanswer in the list.
1=regular outpatient visits with physician (member of MDT)2=follow-up with LCNS3=virtual follow-up after imaging4=telephone contact with patient5=referred back to primary care doctor0=no follow-up999=don't know
How was relapse detected? Numerical code 0=planned imaging1=symptoms2=incidental finding with unrelated problem999=don't know
Continued
https://doi.org/10.1183/13993003.00610-2018 15
ERS STATEMENT | A.L. RICH ET AL.
patient group felt only a subset of the questions were relevant. This questionnaire should be completed atdiagnosis, after completion of first-line treatment and at 6 months post-diagnosis. This may be difficult toachieve but QoL for patients is a fundamental outcome measure, often neglected. Members of our PAGfelt that ideally we would also collect QoL data at 12 months and after 5-year survival, where applicable. Arevised QoL questionnaire is in development, which incorporates elements of the QLQ-C30 with specificreference to side effects from medical treatments including chemotherapy and targeted therapies [59].
Lung cancer pathway/outcomesThe final section of the European recommended minimum dataset relates to aspects of the lung cancerpathway, specifically the outcomes in terms of treatment and survival (table 4). Patients in some countrieshave identified how important contact with a LCNS is because they provide significant support to patientsand their families throughout the lung cancer pathway. Although there is no accepted internationaldefinition for a LCNS, the task force suggests the following: a LCNS is one whose primary role is to meetindividuals with lung cancer at diagnosis, sometimes before, and then to provide support to the patientand their family in terms of education, access to benefits, liaising with primary care physicians and
TABLE 4 Continued
Data item Definition Detailed definition
Subsequent treatment to lungprimary
Numerical code More than one treatment option can be chosen during thepatient treatment programme (please confirm with datesbelow)
1=surgery2=chemotherapy and radiotherapy in addition to surgery(tri-modality treatment)
3=hyperfractionated radiotherapy4=external beam radiotherapy (curative intent but not CHART)5=stereotactic radiotherapy (3–8 fractions)6=radiofrequency/microwave ablation7=brachytherapy8=palliative radiotherapy to lung primary9=concurrent chemoradiotherapy10=sequential chemoradiotherapy11=palliative chemotherapy12=targeted/biological therapy (TKI etc.)13=immunotherapy14=interventional bronchoscopy15=specialist palliative care999=don't know/not recorded
Date of surgery dd/mm/yyyy
Date of first radiotherapy session dd/mm/yyyy
Nature of radiotherapy Total dose given (Grey) Absolute number (e.g. 30)Number of fractions given Absolute number (e.g. 6)Number of days of radiotherapytreatment
Absolute number (e.g. 12)
Date of first chemotherapy dose dd/mm/yyyy
Date of last chemotherapy dose dd/mm/yyyy
Date of interventional bronchoscopy dd/mm/yyyy
Date of specialist palliative care dd/mm/yyyy Date of first appointment with specialist palliative care physician
Clinical trial Is the patient part of a clinical trial?Numerical code
0=no1=yes999=don't know
Date of death dd/mm/yyyy
Data items in roman are mandatory within the proposed minimum dataset; data items in italics are desirable within the dataset. LCNS: lungcancer nurse specialist; MDT: multidisciplinary team; CHART: continuous hyperfractionated accelerated radiotherapy treatment; dd/mm/yyyy:date, month, year; IASLC: International Association for the Study of Lung Cancer; SABR: stereotactic ablative radiotherapy; SVCO: superior venacava obstruction.
https://doi.org/10.1183/13993003.00610-2018 16
ERS STATEMENT | A.L. RICH ET AL.
emotional support. The role may include other duties, such as administering chemotherapy, although thisdoes not on its own meet the essential elements of holistic care described above.
Treatment data items are shown in table 4 and provide a comprehensive list of treatment options andassociated secondary questions, which would not apply to all cases. In order for meaningful analysis oflung cancer outcomes to take place, and the influence of treatment modalities on survival to be assessed,every effort must be made to capture all relevant information.
Part 2. Manual of standards for lung cancer services in EuropePublications defining lung cancer service specification had variable content. Four broad areas wereidentified that distinguished them:
• geographic scope (international, national or regional setting);• comprehensiveness of care (comprehensive cancer services, lung cancer-specific services and services
that provide only selected diagnostic or treatment modalities);• publishing body, such as national or international healthcare authorities or medical societies, insurance
companies or other non-governmental bodies reimbursing costs of care, foundations, or a combinationof these bodies; and
• the time point and up-to-dateness of publication.
No international initiatives could be identified which defined standards of care specifically for the entirelung cancer pathway, although there are two examples of relatively comprehensive cancer care servicedefinitions on the European level. These are the European Society for Medical Oncology DesignatedCentres of Integrated Oncology and Palliative Care accreditation programme, initiated in 2003 [60], andthe Organisation of European Cancer Institutes (OECI) Accreditation and Designation Programme,revised in 2015 [61]. Several international medical societies have published statement papers on standardsfor selected parts of the lung cancer pathway (supplement 1.2).
The US National Cancer Institute (NCI) established the first successful comprehensive cancer centreprogramme in 1971, supported by the National Cancer Act. There are now 69 NCI-designated(Comprehensive) Cancer Centers, all of which have a focus on basic, clinical and population-basedresearch [62]. This has been reviewed in relation to developing centres in Europe to support, primarily,research [63].
The Bonnie J. Addario Lung Cancer Foundation has established its own foundation-based “Centre ofExcellence Program”, currently encompassing 17 community hospitals as well as 17 Addario Lung CancerMedical Institute hospitals in the USA and three in Europe (Paris, France; Torino, Italy; and Barcelona,Spain) [64].
A number of other approaches have been taken to formalise the lung cancer pathway within Europeancountries, and these are described in the paragraphs below.
UKIn 1995, the report by CALMAN and HINE, “A Policy Framework for Commissioning Cancer Services” [65],set the basic standards for cancer services in England and Wales including MDTs working as a coreelement of cancer services. Since then, the NHS has further developed and regularly updated standards ofcancer centre-based care in the UK, and standards have been monitored through a national peer reviewprocess and the NLCA [19, 20, 22]. Furthermore, a national optimal clinical pathway for suspected andconfirmed lung cancer: from referral to treatment” has been published [66]. In 2014, Cancer Research UKnamed the “Lung Cancer Centres of Excellence”, jointly based in London and Manchester, whose aim is todevelop and promote high-level lung cancer research [67].
DenmarkIn Denmark, as mentioned above, the DLCG, through the DLCR and the national lung cancer guidelineprogramme and in collaboration with national healthcare authorities, catalysed a process of continuousimprovement of lung cancer care which has, among other things, instigated a re-organisation withcentralisation of Danish lung cancer services [17]. Supplement 1.4 depicts the lung cancer service in theregion of Southern Denmark.
FranceFrance has a national task force against cancer that has developed three national “cancer plans” [68]. Thefirst cancer plan, launched by President Chirac (2003–2007), set the basis of a national strategy formultidisciplinary management of cancer. It legalised the compulsory multidisciplinary discussion of eachindividual cancer patient. MDTs are organised according to organ or system; within thoracic oncology,
pleural mesothelioma and thymic epithelial tumours fall within the remit of rare tumour boards(national), rather than the lung MDT. The MDT discussion must lead to a consensual personalisedtreatment plan, which is a written document given to the patient during a structured consultation, and anurse coordinator is also present to offer psychological or social support if required. The plan is also sentto the patient’s general practitioner and all corresponding doctors.
The first cancer plan also elaborated on the accreditation of units caring for patients with cancer, and inparticular of surgical units. A surgical unit should host at least two surgeons, have access to an intensivecare unit and an endoscopy suite, and have a frozen section analysis available on site. Minimumthresholds have been set per organ, which result in a minimal caseload of 20 major resections per surgeon(respectively 30 cases per unit, given some surgeons work on more than just cancer).
The Ministry of Health created a national institute of cancer (Institut National du Cancer (INCa)) in 2005,which coordinates research and treatment in oncology. INCa publishes an annual report and collaborateswith 25 regional oncology networks, which coordinate screening and treatment at the regional level. INCais also connected to the Higher Authority of Health (Haute Autorité de la Santé, HAS), which is in chargeof editing guidelines and quality control. Finally, INCa has accredited and coordinates eight inter-groupsfor clinical research, including the French Intergroup of Thoracic Oncology (IFCT).
Two subsequent cancer plans have been launched by presidents Sarkozy (2009–2013) and Hollande(2014–2019). The third cancer plan is an ambitious document [69] that not only aims to improvetreatment, but also to act before diagnosis (prevention, screening) and after treatment (follow-up, socialre-integration).
GermanyIn 2008, the German Cancer Society in collaboration with the German Respiratory Society and theGerman Society of Thoracic Surgery initiated a certification programme for lung cancer centres as part ofthe German National Cancer Plan. In September 2016 there were 44 certified lung cancer centres inGermany and two in Switzerland. The certification process comprises:
• an annual updated parameter manual with mandatory and recommended elements of structure,process and outcome data which are used for self-assessment and subsequent external validation;
• annual visits to the respective lung cancer service by trained external specialists;• an extensive evaluation of the results by an independent institute; and• a final evaluation [70, 71].
The German parameter manual contains 10 chapters covering mainly medical aspects of the lung cancerpathway. Multi-professional/disciplinary working is encouraged and there are specific mandatory standardsfor centres. These include diagnosing and treating ⩾200 new patients with pathologically confirmed lungcancer per year and ⩾75 anatomical lung cancer resections per year, and recording performance indicatorssuch as a ⩽5% 30-day mortality after anatomical lung cancer resections, and ⩾10% proportion ofbroncho-/angioplastic resections on all anatomical resections. Clinical lung cancer registration andfollow-up data collection are mandatory in every certified lung cancer centre and their close linkage to thenewly established clinical cancer registries of the 16 German Federal States is promoted [70, 71]. Theprocess has seen improvements in multidisciplinary working.
Only 33% of all new cases of lung cancer in 2016 were covered by certified lung cancer centres. The mainobstacles for broader implementation are the mandatory thresholds for new cases and surgical resections[70, 71]. Other medical societies in Germany have established independent certification programmesrelated to lung cancer care (i.e. the “Oncological Centres” of the German Society for Haematology andMedical Oncology and the “Thoracic Centres” of the German Society of Thoracic Surgery, the latterinitiative appraising both benign and malignant disease) [72, 73].
Overview of the development of the manual of standards for lung cancer servicesin EuropeThe task force group agreed on the following scope and core principles for developing the parametermanual of European standards for lung cancer services:
1) The primary target audience of the parameter manual is professionals involved in lung cancer care inEurope. The standards will also be important for lung cancer patients, their carers and otherstakeholders in lung cancer care.2) The main aim is to harmonise and improve standards of lung cancer care throughout Europe.Multidisciplinary teamwork and patient-centred care are central.
https://doi.org/10.1183/13993003.00610-2018 18
ERS STATEMENT | A.L. RICH ET AL.
3) The parameter manual is composed of two sections covering i) infrastructure and organisation of thelung cancer service; and ii) standards for lung cancer services at each stage of the lung cancer pathway.4) Standards are divided into essential and advanced. “Essential standards” are defined as criteria whichare mandatory for the lung cancer service to fulfil basic standards of effective care. “Advancedstandards” are defined as those that go beyond that which is essential to provide higher-quality lungcancer care.5) The underlying evidence base for the essential and advanced standards was graded into three levels: i)“Guideline”: wherever possible, generally accepted clinical lung cancer guideline recommendations wereused to conclude standards for the infrastructure or pathway for lung cancer services (i.e. the guidelinerecommendation “Lung cancer patients who are potentially suitable for treatment with curative intentshould be offered PET-CT [positron emission tomography computed tomography] before treatment”led to the essential standard in this manual “The lung cancer service must provide or have accessto PET-CT”; ii) “Literature review and assessment”: these denoted that standards were based on anassessment of the available non-guideline literature; iii) “Good practice”: in the absence of anyguideline recommendations or other literature, task force members and patient representatives usedtheir clinical experience to reach conclusions about what constitutes good clinical practice for certainstandards.6) It is acknowledged that differences in terminology can lead to differences in interpretation acrossEurope; a glossary for the terminology is provided in supplement 3.
The PAG has already formulated patient priorities in lung cancer care, which were published in an ELFreport [74]. These patient priorities comprise proper patient involvement and the provision of relevantand understandable information needed for decision-making; quantitative and qualitative improvement ofpatient–professional contacts throughout the lung cancer pathway; better involvement of other professions,especially lung cancer nurses; supervision and psychological support for doctors and other professionals;specific communication training for professionals; and better linkage between lung cancer services.
Recommendations for a pan-European manual of standards for lung cancerservicesOrganisation of the lung cancer serviceThe manual of standards for a lung cancer service in Europe is provided as supplement 3. This firstsection addresses the relevant organisational aspects of the lung cancer service as a whole. Although amultidisciplinary network environment is an essential requirement, it was agreed that the specificmembership should be determined according to the local and/or national setting. Advanced standardshave been formulated to encourage lung cancer services that have a full range of diagnostic and/ortreatment facilities to offer these to partner organisations. It is important to note that there is no oneinfrastructure that every service should adopt. Every aspect of the lung cancer pathway should be availableto the individual patient, but the delivery of this may vary at the local level. A real-life example of amulti-site lung cancer service from Denmark is included in supplement 1.4.
The PAG also elaborated on the standards for patient- and carer-centred care. The evidence base for thisis limited, although not strictly necessary when a patient expert group has commented and when there areseveral national lung cancer guidelines recommending shared decision-making on the basis of informationthat is easy to access and understand [75].
The task force identified further “essential standards” in a lung cancer service which relate to:
• adherence to evidence-based care, with use of regularly updated guidelines;• access to specialised care;• timeliness of care;• documentation, accessibility and provision of patient and carer-related information;• communication and environment for communication;• education for healthcare professionals, patients and carers (e.g. the Thoracic Oncology HERMES
syllabus and curriculum [76–80]);• clinical cancer registration;• quality assurance, quality improvement and risk management; and• collaboration with external healthcare professionals and other external stakeholders by the lung cancer
service.
The utilisation of the proposed pan-European dataset for lung cancer registration is recommended as anadvanced standard. Advanced collaborative measures have been proposed by the task force group tofacilitate local, regional, national and international networking.
Lung cancer pathwayThe second section of the manual encompasses the entire lung cancer pathway within the lung cancerservice, from diagnosis through treatment, follow-up, relapse and end of life or survivorship (supplement3). The underlying international and national guidelines which provide recommendations related to mostof the essential and advanced standards within this section are listed in supplement 1.2.
Cross-pathway care is included in this section. This is often important to ensure that the patient’sexperience is maximised when care is needed from services outside the lung cancer pathway; these mayinclude emergency care, intensive care and services for specific symptom management. Palliative care isincluded here but it is noted that this should be provided throughout the entire pathway (figure 1) [81].
Pre-existing statement papers and recommendations issued by other international medical societies havebeen reviewed and incorporated into the manual of standards where appropriate. These include imaging[82], fitness for diagnostics and radical therapy [83], thoracic surgery [84], radiotherapy [85–93] andpalliative care [94]. Owing to limited evidence and heterogeneity among and within European countries,the task force group was unable to define standards for individual or institutional volumes of care andtimeliness/waiting times.
The future: implementation of harmonised standards in EuropeThe proposed pan-European lung cancer dataset and manual of standards for lung cancer servicesprovides the opportunity to harmonise registration and quality of services in Europe. A previous ERS taskforce showed marked inequalities in lung cancer care among and within European countries [10], andimportantly established a network of interested clinicians who are ready to be involved with theimplementation of these standards. Thus, we have so far identified variation and reviewed guidelines, andthis paper defines both a pan-European dataset and standards for lung cancer services.
Our proposed standards for lung cancer services and lung cancer registration comprise two essential partsof a lung cancer guideline cycle based on the model originally introduced by the European Commission in2004 (figure 2) [95, 96]. Given the surplus of existing lung cancer guidelines and, as a consequence, thesubstantial waste of human and financial resources, it is imperative that multiple uncoordinated initiativeson the international, national and regional level should be avoided. Therefore, the ERS will seekcollaborations on a par with other leading European societies to define joint pan-European standards forlung cancer services and lung cancer registration based on this statement paper as well asmulti-professional, patient-centred lung cancer guidelines. This would also save valuable resources on thenational and regional level. Given the rapidly evolving field of lung cancer care, these standards will needto be revised on a regular basis to ensure their relevance and efficacy.
Dissemination and implementation of these standards is vital. Although there are some examples ofservice improvement initiated through involvement of individual members of the task force, it is nowimportant to actively manage the process of improving services, care and outcomes throughout Europe.This may be done using methods of service improvement that have been used in individual countriesusing our established network. Peer review is one such established method. This allows individuals andteams to review each other’s services, with reference to agreed standards [97]. In the European setting thisprocess could really drive up standards of care. The peer review process will involve clinicians visiting andevaluating services that may be very different, with the opportunity to suggest some profoundly helpfulchanges and to learn from one another. Following a recent feasibility project benchmarking lungcancer services in Glasgow and Berlin, the ERS will endeavour to support peer review projects on apan-European scale.
In summary, the task forces of the ERS Thoracic Oncology Assembly have so far provided importantinformation about the variation in lung cancer care in a range of European countries with marked
Follow-upThoracic surgery
Palliative care
Diagnostics
Diagnostic period Follow-up period End of life period
or survivorship
Therapeutic period (first line and relapse)
Radiotherapy
Systemic therapy
FIGURE 1 Novel integrated lung cancer care concept with diagnostics, systemic therapy, radiotherapy, surgery, palliative care and follow-up asequitable pillars of lung cancer care. Adapted from [81].
differences in social and political backgrounds. The next phase is to start the process of serviceimprovement, while acknowledging the variable resources available in individual countries. It is envisagedthat this current task force project will form the basis of a multinational, multi-society and patient-centredlung cancer care collaboration with the clear aim to improve and harmonise standards of lung cancer carefor the benefit of patients, their carers and professionals alike.
Acknowledgements: The task force would like to thank members of the European Lung Foundation lung cancer patientadvisory group who provided valuable feedback on both aspects of this project. Specifically, we would like to recognisethe collaboration of Blanka Čepická (Czech Republic), Margaret Gould (UK), Vagn Jespersen (Denmark), TerryKavanagh (UK), Ewelina Szmytke (Poland), Stefania Vallone (Italy), Dan Smyth (Ireland), Janette Rawlinson (UK) andTom Simpson (UK).
Conflict of interest: A.L. Rich has nothing to disclose. D.R. Baldwin reports personal fees for lecturing fromAstraZeneca, outside the submitted work. P. Beckett has nothing to disclose. T. Berghmans has nothing to disclose.J. Boyd is an employee of the European Lung Foundation. C. Faivre-Finn reports research funding and businesstravel support from Merck, AstraZeneca and Pfizer, outside the submitted work. F. Galateau Salle has nothing todisclose. F. Gamarra has nothing to disclose. B. Grigoriu has nothing to disclose. N-C.G. Hansen has nothingto disclose. G. Hardavella has nothing to disclose. E. Jakobsen has nothing to disclose. D. Jovanovic has nothing todisclose. A. Konsoulova has nothing to disclose. G. Massard has nothing to disclose. J. McPhelim reports personal feesfrom Roche, MSD, Pfizer, Lilly Oncology and Abbvie, outside the submitted work. A-P. Meert has nothing to disclose.R. Milroy has nothing to disclose. L. Mutti has nothing to disclose. M. Paesmans has nothing to disclose. M.D. Peakehas nothing to disclose. P.M. Putora has nothing to disclose. D.K.M. de Ruysscher has nothing to disclose. J-P. Sculierhas nothing to disclose. A. Scherpereel has nothing to disclose. D.R. Subotic has nothing to disclose. P. Van Schil hasnothing to disclose. T.G. Blum has nothing to disclose.
References1 Verdecchia A, Francisci S, Brenner H, et al. Recent cancer survival in Europe: a 2000–02 period analysis of
EUROCARE-4 data. Lancet Oncol 2007; 8: 784–796.2 Albreht T, McKee M, Alexe DM, et al. Making progress against cancer in Europe in 2008. Eur J Cancer 2008; 44:
1451–1456.3 Oudkerk M, Devaraj A, Vliegenthart R, et al. European position statement on lung cancer screening. Lancet Oncol
2017; 18: e754–e766.4 Berrino FSM, Verdecchia A, Capocaccia R, et al. Survival of Cancer Patients in Europe. The EUROCARE Study.
Lyon, IARC Scientific Publications, 1995.5 De Angelis R, Sant M, Coleman MP, et al. Cancer survival in Europe 1999–2007 by country and age: results of
EUROCARE-5 – a population-based study. Lancet Oncol 2014; 15: 23–34.6 Rossi S, Baili P, Capocaccia R, et al. The EUROCARE-5 study on cancer survival in Europe 1999–2007: database,
quality checks and statistical analysis methods. Eur J Cancer 2015; 51: 2104–2119.7 European Partnership for Action Against Cancer. http://ec.europa.eu/health/major_chronic_diseases/diseases/
cancer_en#fragment1 Date last accessed: May 2017.
Lung cancer
guideline
Lung cancer servicesLung cancer registry
Monitoring
Development
Distribution
Guideline cycle
Appraisal
ImplementationEvaluation
FIGURE 2 Lung cancer guideline cycle. Adapted from [96].
8 Albreht T, Klasuwa R, Van den Bulcke M. European Guide on Quality Improvement in Comprehensive CancerControl. Slovenia, Cancer Control Joint Action, 2017.
9 European Network of Cancer Registries. Recommendations for a Standard Dataset for the European Network ofCancer Registries 2005. Ispra, European Network of Cancer Registries, 2015.
10 Blum TG, Rich A, Baldwin D, et al. The European initiative for quality management in lung cancer care.Eur Respir J 2014; 43: 1254–1277.
11 Rich A BD, Alfageme I, Beckett P, et al. Achieving thoracic oncology data collection in Europe: a precursor studyin 35 countries. BMC Cancer 2018; 18: 1144.
12 Mak KS, van Bommel AC, Stowell C, et al. Defining a standard set of patient-centred outcomes for lung cancer.Eur Respir J 2016; 48: 852–860.
13 Peake TS, Lowe D, Pearson M. Lung cancer: a national comparative audit. London, Royal College of Physicians, 1999.14 The National Danish Health Authority. Referenceprogram Lungecancer Undersøgelse og behandling [Reference
programme lung cancer: study and treatment]. 1998. www.lungecancer.dk/00164/ Date last updated: October 18,2018.
15 Jakobsen E, Rasmussen TR. The Danish Lung Cancer Registry. Clin Epidemiol 2016; 8: 537–541.16 Jakobsen E, Rasmussen TR, Green A. Mortality and survival of lung cancer in Denmark: results from the Danish
Lung Cancer Group 2000-2012. Acta Oncol 2016; 55: Suppl. 2, 2–9.17 Jakobsen E, Green A, Oesterlind K, et al. Nationwide quality improvement in lung cancer care: the role of the
Danish Lung Cancer Group and Registry. J Thorac Oncol 2013; 8: 1238–1247.18 Danish Lung Cancer Group. 2017. Visionsprojekt Lungekraeft Konferencerapport [Visions Project lung cancer
conference report]. www.lungecancer.dk/documents/F1BFDA1D-EBFD-409A-A26A-15FF5385F00A.pdf.19 Royal College of Physicians. Lung Cancer: a Core Dataset. 2nd Edn. London, Royal College of Physicians, 1999.20 Beckett P, Woolhouse I, Stanley R, et al. Exploring variations in lung cancer care across the UK – the “story so
far” for the National Lung Cancer Audit. Clin Med (Lond) 2012; 12: 14–18.21 Powell HA, Baldwin DR. Multidisciplinary team management in thoracic oncology: more than just a concept?
Eur Respir J 2014; 43: 1776–1786.22 The Healthcare Quality Improvement Partnership. National Lung Cancer Audit 2010. Leeds, NHS Health and
Social Care Information Centre, 2010.23 Royal College of Physicians. National Lung Cancer Audit annual report 2016. London, Royal College of
Physicians, 2017.24 NHS Health and Social Care Information Centre. National Lung Cancer Audit. Leeds, NHS Health and Social
Care Information Centre, 2006.25 Royal College of Physicians. The National Lung Cancer Audit. www.rcplondon.ac.uk/projects/
national-lung-cancer-audit Date last accessed: June 2018.26 Walters S, Benitez-Majano S, Muller P, et al. Is England closing the international gap in cancer survival? Br J
Cancer 2015; 113: 848–860.27 Bergman B, Aaronson NK, Ahmedzai S, et al. The EORTC QLQ-LC13: a modular supplement to the EORTC
Core Quality of Life Questionnaire (QLQ-C30) for use in lung cancer clinical trials. EORTC Study Group onQuality of Life. Eur J Cancer 1994; 30A: 635–642.
28 Basch E, Iasonos A, Barz A, et al. Long-term toxicity monitoring via electronic patient-reported outcomes inpatients receiving chemotherapy. J Clin Oncol 2007; 25: 5374–5380.
29 Midha A, Dearden S, McCormack R. EGFR mutation incidence in non-small-cell lung cancer of adenocarcinomahistology: a systematic review and global map by ethnicity (mutMapII). Am J Cancer Res 2015; 5: 2892–2911.
30 Dearden S, Stevens J, Wu YL, et al. Mutation incidence and coincidence in non small-cell lung cancer:meta-analyses by ethnicity and histology (mutMap). Ann Oncol 2013; 24: 2371–2376.
31 Page BJ, Bowman RV, Yang IA, et al. A survey of lung cancer in rural and remote Aboriginal and Torres StraitIslander communities in Queensland: health views that impact on early diagnosis and treatment. Intern Med J2016; 46: 171–176.
32 Gibberd A, Supramaniam R, Dillon A, et al. Lung cancer treatment and mortality for Aboriginal people in NewSouth Wales, Australia: results from a population-based record linkage study and medical record audit. BMCCancer 2016; 16: 289.
33 Department of Health. Cancer Reform Strategy: Equality Impact Assessment. London, Department of Health, 2007.34 Rich AL, Tata LJ, Stanley RA, et al. Lung cancer in England: information from the National Lung Cancer Audit
(LUCADA). Lung Cancer 2011; 72: 16–22.35 Denton EJ, Hart D, Russell PA, et al. Lung cancer and socio-economic status: inextricably linked to place of
residence. Intern Med J 2017; 47: 563–569.36 Tannenbaum SL, Koru-Sengul T, Zhao W, et al. Survival disparities in non-small cell lung cancer by race,
ethnicity, and socioeconomic status. Cancer J 2014; 20: 237–245.37 Crawford SM, Atherton F. Lung cancer: histological aspects of diagnosis in England and the south east
Netherlands. J Epidemiol Community Health 1994; 48: 420–421.38 Crawford SM, Sauerzapf V, Haynes R, et al. Social and geographical factors affecting access to treatment of lung
cancer. Br J Cancer 2009; 101: 897–901.39 Maclay JD, Farley JM, McCowan C, et al. Obtaining tissue diagnosis in lung cancer patients with poor
performance status and its influence on treatment and survival. Respir Med 2017; 124: 30–35.40 Khakwani A, Rich AL, Tata LJ, et al. The pathological confirmation rate of lung cancer in England using the
NLCA database. Lung Cancer 2013; 79: 125–131.41 Travis WD, Brambilla E, Burke AP, et al. Introduction to The 2015 World Health Organization Classification of
Tumors of the Lung, Pleura, Thymus, and Heart. J Thorac Oncol 2015; 10: 1240–1242.42 Travis WD, Brambilla E, Noguchi M, et al. International Association for the Study of Lung Cancer/American
Thoracic Society/European Respiratory Society international multidisciplinary classification of lungadenocarcinoma. J Thorac Oncol 2011; 6: 244–285.
43 Goldstraw P, Chansky K, Crowley J, et al. The IASLC Lung Cancer Staging Project: proposals for revision of theTNM stage groupings in the forthcoming (eighth) edition of the TNM classification for lung cancer. J ThoracOncol 2016; 11: 39–51.
44 Robinson LA, Ruckdeschel JC, Wagner H Jr, et al. Treatment of non-small cell lung cancer-stage IIIA: ACCPevidence-based clinical practice guidelines (2nd edition). Chest 2007; 132: 3 Suppl., 243S–265S.
45 Asamura H, Chansky K, Crowley J, et al. The International Association for the Study of Lung Cancer LungCancer Staging Project: proposals for the revision of the N descriptors in the forthcoming 8th edition of the TNMclassification for lung cancer. J Thorac Oncol 2015; 10: 1675–1684.
46 Oken MM, Creech RH, Tormey DC, et al. Toxicity and response criteria of the Eastern Cooperative OncologyGroup. Am J Clin Oncol 1982; 5: 649–655.
47 Rich AL, Tata LJ, Free CM, et al. Inequalities in outcomes for non-small cell lung cancer: the influence of clinicalcharacteristics and features of the local lung cancer service. Thorax 2011; 66: 1078–1084.
48 Rich AL, Tata LJ, Free CM, et al. How do patient and hospital features influence outcomes in small-cell lungcancer in England? Br J Cancer 2011; 105: 746–752.
49 Kawaguchi T, Takada M, Kubo A, et al. Performance status and smoking status are independent favorableprognostic factors for survival in non-small cell lung cancer: a comprehensive analysis of 26,957 patients withNSCLC. J Thorac Oncol 2010; 5: 620–630.
50 Reck M, Thatcher N, Smit EF, et al. Baseline quality of life and performance status as prognostic factors inpatients with extensive-stage disease small cell lung cancer treated with pemetrexed plus carboplatin versusetoposide plus carboplatin. Lung Cancer 2012; 78: 276–281.
51 Edwards BK, Noone AM, Mariotto AB, et al. Annual Report to the Nation on the status of cancer, 1975–2010,featuring prevalence of comorbidity and impact on survival among persons with lung, colorectal, breast, orprostate cancer. Cancer 2014; 120: 1290–1314.
52 Grose D, Morrison DS, Devereux G, et al. The impact of comorbidity upon determinants of outcome in patientswith lung cancer. Lung Cancer 2015; 87: 186–192.
53 Islam KM, Jiang X, Anggondowati T, et al. Comorbidity and survival in lung cancer patients. Cancer EpidemiolBiomarkers Prev 2015; 24: 1079–1085.
54 Luchtenborg M, Jakobsen E, Krasnik M, et al. The effect of comorbidity on stage-specific survival in resectednon-small cell lung cancer patients. Eur J Cancer 2012; 48: 3386–3395.
55 Charlson ME, Pompei P, Ales KL, et al. A new method of classifying prognostic comorbidity in longitudinalstudies: development and validation. J Chronic Dis 1987; 40: 373–383.
56 Piccirillo JF CI, Claybour P, Borah AJ, et al. The measurement of comorbidity by cancer registries. J RegistryManag 2003; 30: 8–14.
57 Sangha O, Stucki G, Liang MH, et al. The Self-Administered Comorbidity Questionnaire: a new method to assesscomorbidity for clinical and health services research. Arthritis Rheum 2003; 49: 156–163.
58 Koller M, Warncke S, Hjermstad MJ, et al. Use of the lung cancer-specific quality of life questionnaire EORTCQLQ-LC13 in clinical trials: a systematic review of the literature 20 years after its development. Cancer 2015; 121:4300–4323.
59 Koller M, Hjermstad MJ, Tomaszewski KA, et al. An international study to revise the EORTC questionnaire forassessing quality of life in lung cancer patients. Ann Oncol 2017; 28: 2874–2881.
60 European Society for Medical Oncology. Designated Centres of Integrated Oncology and Palliative CareApplication 2016. http://esmo.org/Patients/Designated-Centres-of-Integrated-Oncology-and-Palliative-Care Datelast accessed: November 27, 2017.
61 Organisation of European Cancer Institutes. OECI Accreditation and Designation 2015. www.oeci.eu/Attachments/OECI_ACC_Manual_2_0.pdf Date last accessed: November 27, 2017.
62 National Cancer Institute. NCI-Designated Cancer Centers 2017. www.cancer.gov/research/nci-role/cancer-centersDate last accessed: November 27, 2017.
63 Sullivan R. Has the US Cancer Centre model been “successful”? Lessons for the European cancer community. MolOncol 2009; 3: 192–203.
64 Bonnie J. Addario Lung Cancer Foundation. Centers of Excellence 2017. www.lungcancerfoundation.org/patients/centers-of-excellence/ Date last accessed: November 27, 2017.
65 Calman K, Hine D. A Policy Framework for Commissioning Cancer Services. A Report by the Expert AdvisoryGroup on Cancer to the Chief Medical Officers of England and Wales. London, Department of Health, 1995.
66 Lung Clinical Expert Group. 2017. National Optimal Lung Cancer Pathway. www.cancerresearchuk.org/sites/default/files/national_optimal_lung_pathway_aug_2017.pdf Date last accessed: November 27, 2017.
67 Cancer Research UK. Lung Cancer Centres of Excellence 2017. www.cruklungcentre.org/ Date last accessed:November 27, 2017.
68 Khayat D. National cancer plans: the French experience. Am Soc Clin Oncol Educ Book 2013; 33: e242–e244.69 The National Institute of Cancer, France. The Cancer Plan 2017–2019 http://en.e-cancer.fr/The-Cancer-
Plan-2014-2019 Data last accessed: November 27, 2017. Date last updated: October 5, 2015.70 Ukena DH H, Bischofsberger A, Ferencz J, et al. Lungenkrebszentren - Entwicklung und aktueller Status [Lung
cancer centres - development and current status]. Pneumologe 2017; 14: 61–73.71 OnkoZert. Informationen Zertifizierung Lungenkrebszentren [Certification information lung cancer centres].
http://onkozert.de/lungenkrebszentren.htm Date last accessed: November 27, 2017.72 Deutsch Gesellschaft für Thoraxchirurgie. Kompetenzzentrum Thoraxchirurgie [Competent centres in thoracic
surgery]. www.dgt-online.de/fuer-aerzte-kliniken/zertifizierung/ Date last accessed: November 27, 2017.73 Deutsch Gesellschaft für Hämatologie und Medinzinische Onkologie. Zertifizierungen [Certification]. 2017. www.
onkologie-zertifizierung.de/ Date last accessed: November 27, 2017.74 Boyd J. Patient priorities project: lung cancer - consultation activities report. European Lung Foundation Internal
Report 2015. Sheffield, European Lung Foundation, 2015.75 European Lung Foundation. 2015. Patient priorities project: lung cancer - consultation activities report 2015.
www.europeanlunginfo.org/lung-cancer/research-and-news/report-on-consultation-lung-cancer-patient-priorities-reportDate last accessed: November 27, 2017.
76 Gamarra F, Noel JL, Brunelli A, et al. Thoracic oncology HERMES: European curriculum recommendations fortraining in thoracic oncology. Breathe 2016; 12: 249–255.
77 Meert AP, Noel JL, Gamarra F, et al. The thoracic oncology specialist: curriculum recommendations in thoraciconcology training. Eur Respir J 2016; 48: 628–631.
78 Gamarra F, Boffetta P, De Ruysscher D, et al. Thoracic oncology HERMES syllabus: setting the basis for thoraciconcology training in Europe. Eur Respir J 2013; 42: 568–571.
79 Massard G, Antonoff MB, Noel JL, et al. Transatlantic editorial: thoracic surgeons need recognition of competencein thoracic oncology. Eur J Cardiothorac Surg 2017; 52: 611–615.
80 Massard G, Antonoff MB, Noel JL, et al. Transatlantic editorial: thoracic surgeons need recognition of competencein thoracic oncology. Ann Thorac Surg 2017; 104: 1103–1107.
81 Blum T, Schonfeld N. The lung cancer patient, the pneumologist and palliative care: a developing alliance.Eur Respir J 2015; 45: 211–226.
82 European Society of Radiology, American College of Radiology. European Society of Radiology (ESR) andAmerican College of Radiology (ACR) report of the 2015 global summit on radiological quality and safety. InsightsImaging 2016; 7: 481–484.
83 Brunelli A, Charloux A, Bolliger CT, et al. The European Respiratory Society and European Society of ThoracicSurgeons clinical guidelines for evaluating fitness for radical treatment (surgery and chemoradiotherapy) inpatients with lung cancer. Eur J Cardiothorac Surg 2009; 36: 181–184.
84 Brunelli A, Falcoz PE, D’Amico T, et al. European guidelines on structure and qualification of general thoracicsurgery. Eur J Cardiothorac Surg 2014; 45: 779–786.
85 Matsuo Y, Onishi H, Nakagawa K, et al. Guidelines for respiratory motion management in radiation therapy.J Radiat Res 2013; 54: 561–568.
86 Boily G, Filion E, Rakovich G, et al. Stereotactic ablative radiation therapy for the treatment of early-stagenon-small-cell lung cancer: CEPO review and recommendations. J Thorac Oncol 2015; 10: 872–882.
87 Guckenberger M, Andratschke N, Alheit H, et al. Definition of stereotactic body radiotherapy: principles andpractice for the treatment of stage I non-small cell lung cancer. Strahlenther Onkol 2014; 190: 26–33.
88 Sahgal A, Roberge D, Schellenberg D, et al. The Canadian Association of Radiation Oncology scope ofpractice guidelines for lung, liver and spine stereotactic body radiotherapy. Clin Oncol (R Coll Radiol) 2012; 24:629–639.
89 Kirkbride P, Cooper T. Stereotactic body radiotherapy. Guidelines for commissioners, providers and clinicians: anational report. Clin Oncol (R Coll Radiol) 2011; 23: 163–164.
90 Benedict SH, Yenice KM, Followill D, et al. Stereotactic body radiation therapy: the report of AAPM Task Group101. Med Phys 2010; 37: 4078–4101.
91 De Ruysscher D, Faivre-Finn C, Moeller D, et al. European Organization for Research and Treatment of Cancer(EORTC) recommendations for planning and delivery of high-dose, high precision radiotherapy for lung cancer.Radiother Oncol 2017; 124: 1–10.
92 Potters L, Kavanagh B, Galvin JM, et al. American Society for Therapeutic Radiology and Oncology (ASTRO) andAmerican College of Radiology (ACR) practice guideline for the performance of stereotactic body radiationtherapy. Int J Radiat Oncol Biol Phys 2010; 76: 326–332.
93 Guckenberger M, Andratschke N, Dieckmann K, et al. ESTRO ACROP consensus guideline on implementationand practice of stereotactic body radiotherapy for peripherally located early stage non-small cell lung cancer.Radiother Oncol 2017; 124: 11–17.
94 European Association for Palliative Care. White Paper on Standards and Norms for Hospice and Palliative Care inEurope: part 1+2. www.eapcnet.eu/publications/Organisation/EAPCStandardsNorms Date last accessed: November4, 2017.
95 European Commission. Aid Delivery Methods. Volume 1. Project Cycle Management Guidelines. Brussels,European Commission. 2004. https://ec.europa.eu/europeaid/sites/devco/files/methodology-aid-delivery-methods-project-cycle-management-200403_en_2.pdf Date last accessed: November 27, 2017.
96 Blum TG, Schönfeld N, Jagota A, et al. Integration und Steuerfunktion klinischer Krebsregister in deronkologischen Versorgung [Integration and control function of clinical cancer registries in oncological care].Forum 2012; 27: 431–435.
97 Russell GK, Jimenez S, Martin L, et al. A multicentre randomised controlled trial of reciprocal lung cancer peerreview and supported quality improvement: results from the improving lung cancer outcomes project. Br J Cancer2014; 110: 1936–1942.
![SERIES ‘‘ATS/ERS TASK FORCE: STANDARDISATION OF LUNG … · 2013. 5. 2. · Respiratory Society (ERS) statements [5, 7, 8]. Height and weight should be measured for each patient](https://static.documents.pub/doc/80x56/5fc9742a355705549e03215d/series-aaatsers-task-force-standardisation-of-lung-2013-5-2-respiratory.jpg)
